Arginine deiminase augments the chemosensitivity of argininosuccinate synthetase-deficient pancreatic cancer cells to gemcitabine via inhibition of NF-κB signaling

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Liu, Jiangbo ^a,b   Ma, Jiguang ^a   Wu, Zheng ^a   Li, Wei ^a   Zhang, Dong ^a   Han, Liang ^a   Wang, Fengfei ^c   Reindl, Katie M ^c   Wu, Erxi ^c   Ma, Qingyong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE DEIMINASE; ARGININOSUCCINATE SYNTHASE; CASPASE 3; CASPASE 9; GEMCITABINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SURVIVIN; SYNAPTOTAGMIN I; DEOXYCYTIDINE; HYDROLASE; PROTEIN KINASE B; STAT3 PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR INVASION; TUMOR XENOGRAFT; UPREGULATION; VERY ELDERLY; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; CANCER GRADING; CANCER STAGING; CELL CYCLE; CELL NUCLEUS; CELL TRANSFORMATION; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION; GENETICS; METABOLISM; METASTASIS; MIDDLE AGED; PANCREAS TUMOR; PATHOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR VOLUME;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; ARGININOSUCCINATE SYNTHASE; CELL CYCLE; CELL LINE, TUMOR; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; DEOXYCYTIDINE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; HUMANS; HYDROLASES; MALE; MICE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM METASTASIS; NEOPLASM STAGING; NF-KAPPA B; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84907387232     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-686     Document Type: Article

References (54)

1. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet 2011, 378(9791):607-620. 10.1016/S0140-6736(10)62307-0, 21620466.
2. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014, 64(1):9-29. 10.3322/caac.21208, 24399786.
3. Raimondi S, Maisonneuve P, Lowenfels AB. Epidemiology of pancreatic cancer: an overview. Nat Rev Gastroenterol Hepatol 2009, 6(12):699-708. 10.1038/nrgastro.2009.177, 19806144.
4. Cascinu S, Berardi R, Labianca R, Siena S, Falcone A, Aitini E, Barni S, Di Costanzo F, Dapretto E, Tonini G, Pierantoni C, Artale S, Rota S, Floriani I, Scartozzi M, Zaniboni A. Cetuximab plus gemcitabine and cisplatin compared with gemcitabine and cisplatin alone in patients with advanced pancreatic cancer: a randomised, multicentre, phase II trial. Lancet Oncol 2008, 9(1):39-44. 10.1016/S1470-2045(07)70383-2, 18077217.
5. Nakai Y, Isayama H, Sasaki T, Sasahira N, Tsujino T, Toda N, Kogure H, Matsubara S, Ito Y, Togawa O, Arizumi T, Hirano K, Tada M, Omata M, Koike K. A multicentre randomised phase II trial of gemcitabine alone vs gemcitabine and S-1 combination therapy in advanced pancreatic cancer: GEMSAP study. Br J Cancer 2012, 106(12):1934-1939. 10.1038/bjc.2012.183, 3388559, 22555398.
6. Tuinmann G, Hegewisch-Becker S, Zschaber R, Kehr A, Schulz J, Hossfeld DK. Gemcitabine and mitomycin C in advanced pancreatic cancer: a single-institution experience. Anticancer Drugs 2004, 15(6):575-579. 10.1097/01.cad.0000131683.29260.d1, 15205599.
7. Barbul A. Arginine: biochemistry, physiology, and therapeutic implications. JPEN J Parenter Enteral Nutr 1986, 10(2):227-238. 10.1177/0148607186010002227, 3514981.
8. Ensor CM, Holtsberg FW, Bomalaski JS, Clark MA. Pegylated arginine deiminase (ADI-SS PEG20,000 mw) inhibits human melanomas and hepatocellular carcinomas in vitro and in vivo. Cancer Res 2002, 62(19):5443-5450.
9. Kelly MP, Jungbluth AA, Wu BW, Bomalaski J, Old LJ, Ritter G. Arginine deiminase PEG20 inhibits growth of small cell lung cancers lacking expression of argininosuccinate synthetase. Br J Cancer 2012, 106(2):324-332. 10.1038/bjc.2011.524, 3261683, 22134507.
10. Yoon CY, Shim YJ, Kim EH, Lee JH, Won NH, Kim JH, Park IS, Yoon DK, Min BH. Renal cell carcinoma does not express argininosuccinate synthetase and is highly sensitive to arginine deprivation via arginine deiminase. Int J Cancer 2007, 120(4):897-905. 10.1002/ijc.22322, 17096330.
11. Kim RH, Coates JM, Bowles TL, McNerney GP, Sutcliffe J, Jung JU, Gandour-Edwards R, Chuang FY, Bold RJ, Kung HJ. Arginine deiminase as a novel therapy for prostate cancer induces autophagy and caspase-independent apoptosis. Cancer Res 2009, 69(2):700-708. 10.1158/0008-5472.CAN-08-3157, 2629384, 19147587.
12. Takaku H, Takase M, Abe S, Hayashi H, Miyazaki K. In vivo anti-tumor activity of arginine deiminase purified from Mycoplasma arginini. Int J Cancer 1992, 51(2):244-249. 10.1002/ijc.2910510213, 1568792.
13. Feun LG, Marini A, Walker G, Elgart G, Moffat F, Rodgers SE, Wu CJ, You M, Wangpaichitr M, Kuo MT, Sisson W, Jungbluth AA, Bomalaski J, Savaraj N. Negative argininosuccinate synthetase expression in melanoma tumours may predict clinical benefit from arginine-depleting therapy with pegylated arginine deiminase. Br J Cancer 2012, 106(9):1481-1485. 10.1038/bjc.2012.106, 3341859, 22472884.
14. Shen LJ, Beloussow K, Shen WC. Modulation of arginine metabolic pathways as the potential anti-tumor mechanism of recombinant arginine deiminase. Cancer Lett 2006, 231(1):30-35. 10.1016/j.canlet.2005.01.007, 16356828.
15. Bowles TL, Kim R, Galante J, Parsons CM, Virudachalam S, Kung HJ, Bold RJ. Pancreatic cancer cell lines deficient in argininosuccinate synthetase are sensitive to arginine deprivation by arginine deiminase. Int J Cancer 2008, 123(8):1950-1955. 10.1002/ijc.23723, 18661517.
16. Burris HR, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, Nelson R, Dorr FA, Stephens CD, Von Hoff DD. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 1997, 15(6):2403-2413.
17. Mukherjee S, Hurt CN, Bridgewater J, Falk S, Cummins S, Wasan H, Crosby T, Jephcott C, Roy R, Radhakrishna G, McDonald A, Ray R, Joseph G, Staffurth J, Abrams RA, Griffiths G, Maughan T. Gemcitabine-based or capecitabine-based chemoradiotherapy for locally advanced pancreatic cancer (SCALOP): a multicentre, randomised, phase 2 trial. Lancet Oncol 2013, 14(4):317-326. 10.1016/S1470-2045(13)70021-4, 3620899, 23474363.
18. Karnitz LM, Flatten KS, Wagner JM, Loegering D, Hackbarth JS, Arlander SJ, Vroman BT, Thomas MB, Baek YU, Hopkins KM, Lieberman HB, Chen J, Cliby WA, Kaufmann SH. Gemcitabine-induced activation of checkpoint signaling pathways that affect tumor cell survival. Mol Pharmacol 2005, 68(6):1636-1644.
19. Kagawa S, Takano S, Yoshitomi H, Kimura F, Satoh M, Shimizu H, Yoshidome H, Ohtsuka M, Kato A, Furukawa K, Matsushita K, Nomura F, Miyazaki M. Akt/mTOR signaling pathway is crucial for gemcitabine resistance induced by Annexin II in pancreatic cancer cells. J Surg Res 2012, 178(2):758-767. 10.1016/j.jss.2012.05.065, 22726648.
20. Shrikhande SV, Kleeff J, Kayed H, Keleg S, Reiser C, Giese T, Buchler MW, Esposito I, Friess H. Silencing of X-linked inhibitor of apoptosis (XIAP) decreases gemcitabine resistance of pancreatic cancer cells. Anticancer Res 2006, 26(5A):3265-3273.
21. Singh S, Srivastava SK, Bhardwaj A, Owen LB, Singh AP. CXCL12-CXCR4 signalling axis confers gemcitabine resistance to pancreatic cancer cells: a novel target for therapy. Br J Cancer 2010, 103(11):1671-1679. 10.1038/sj.bjc.6605968, 2994230, 21045835.
22. Bafna S, Kaur S, Momi N, Batra SK. Pancreatic cancer cells resistance to gemcitabine: the role of MUC4 mucin. Br J Cancer 2009, 101(7):1155-1161. 10.1038/sj.bjc.6605285, 2768097, 19738614.
23. Arlt A, Gehrz A, Muerkoster S, Vorndamm J, Kruse ML, Folsch UR, Schafer H. Role of NF-kappaB and Akt/PI3K in the resistance of pancreatic carcinoma cell lines against gemcitabine-induced cell death. Oncogene 2003, 22(21):3243-3251. 10.1038/sj.onc.1206390, 12761494.
24. Zheng C, Jiao X, Jiang Y, Sun S. ERK1/2 activity contributes to gemcitabine resistance in pancreatic cancer cells. J Int Med Res 2013, 41(2):300-306. 10.1177/0300060512474128, 23569008.
25. Sizemore N, Leung S, Stark GR. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol Cell Biol 1999, 19(7):4798-4805. 84278, 10373529.
26. Madrid LV, Mayo MW, Reuther JY, Baldwin AJ. Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 2001, 276(22):18934-18940. 10.1074/jbc.M101103200, 11259436.
27. Huang XY, Wang HC, Yuan Z, Li A, He ML, Ai KX, Zheng Q, Qin HL. Gemcitabine combined with gum mastic causes potent growth inhibition and apoptosis of pancreatic cancer cells. Acta Pharmacol Sin 2010, 31(6):741-745. 10.1038/aps.2010.54, 4002976, 20523344.
28. Kong R, Sun B, Jiang H, Pan S, Chen H, Wang S, Krissansen GW, Sun X. Downregulation of nuclear factor-kappaB p65 subunit by small interfering RNA synergizes with gemcitabine to inhibit the growth of pancreatic cancer. Cancer Lett 2010, 291(1):90-98. 10.1016/j.canlet.2009.10.001, 19880242.
29. Pan X, Arumugam T, Yamamoto T, Levin PA, Ramachandran V, Ji B, Lopez-Berestein G, Vivas-Mejia PE, Sood AK, McConkey DJ, Logsdon CD. Nuclear factor-kappaB p65/relA silencing induces apoptosis and increases gemcitabine effectiveness in a subset of pancreatic cancer cells. Clin Cancer Res 2008, 14(24):8143-8151. 10.1158/1078-0432.CCR-08-1539, 19088029.
30. Uwagawa T, Chiao PJ, Gocho T, Hirohara S, Misawa T, Yanaga K. Combination chemotherapy of nafamostat mesilate with gemcitabine for pancreatic cancer targeting NF-kappaB activation. Anticancer Res 2009, 29(8):3173-3178.
31. Beloussow K, Wang L, Wu J, Ann D, Shen WC. Recombinant arginine deiminase as a potential anti-angiogenic agent. Cancer Lett 2002, 183(2):155-162. 10.1016/S0304-3835(01)00793-5, 12065090.
32. Miyazaki K, Takaku H, Umeda M, Fujita T, Huang WD, Kimura T, Yamashita J, Horio T. Potent growth inhibition of human tumor cells in culture by arginine deiminase purified from a culture medium of a Mycoplasma-infected cell line. Cancer Res 1990, 50(15):4522-4527.
33. Zhang D, Ma QY, Hu HT, Zhang M. beta2-adrenergic antagonists suppress pancreatic cancer cell invasion by inhibiting CREB, NFkappaB and AP-1. Cancer Biol Ther 2010, 10(1):19-29. 10.4161/cbt.10.1.11944, 20424515.
34. Likhite N, Warawdekar UM. A unique method for isolation and solubilization of proteins after extraction of RNA from tumor tissue using trizol. J Biomol Tech 2011, 22(1):37-44. 3059540, 21455480.
35. Liu H, Ma Q, Li J. High glucose promotes cell proliferation and enhances GDNF and RET expression in pancreatic cancer cells. Mol Cell Biochem 2011, 347(1-2):95-101.
36. Albrethsen J, Bogebo R, Gammeltoft S, Olsen J, Winther B, Raskov H. Upregulated expression of human neutrophil peptides 1, 2 and 3 (HNP 1-3) in colon cancer serum and tumours: a biomarker study. BMC Cancer 2005, 5:8. 10.1186/1471-2407-5-8, 548152, 15656915.
37. Dillon BJ, Prieto VG, Curley SA, Ensor CM, Holtsberg FW, Bomalaski JS, Clark MA. Incidence and distribution of argininosuccinate synthetase deficiency in human cancers: a method for identifying cancers sensitive to arginine deprivation. Cancer 2004, 100(4):826-833. 10.1002/cncr.20057, 14770441.
38. Delage B, Fennell DA, Nicholson L, McNeish I, Lemoine NR, Crook T, Szlosarek PW. Arginine deprivation and argininosuccinate synthetase expression in the treatment of cancer. Int J Cancer 2010, 126(12):2762-2772.
39. Hu J, Nakano H, Sakurai H, Colburn NH. Insufficient p65 phosphorylation at S536 specifically contributes to the lack of NF-kappaB activation and transformation in resistant JB6 cells. Carcinogenesis 2004, 25(10):1991-2003. 10.1093/carcin/bgh198, 15192014.
40. Jiang X, Takahashi N, Matsui N, Tetsuka T, Okamoto T. The NF-kappa B activation in lymphotoxin beta receptor signaling depends on the phosphorylation of p65 at serine 536. J Biol Chem 2003, 278(2):919-926. 10.1074/jbc.M208696200, 12419817.
41. Gong H, Pottgen C, Stuben G, Havers W, Stuschke M, Schweigerer L. Arginine deiminase and other antiangiogenic agents inhibit unfavorable neuroblastoma growth: potentiation by irradiation. Int J Cancer 2003, 106(5):723-728. 10.1002/ijc.11298, 12866032.
42. Park IS, Kang SW, Shin YJ, Chae KY, Park MO, Kim MY, Wheatley DN, Min BH. Arginine deiminase: a potential inhibitor of angiogenesis and tumour growth. Br J Cancer 2003, 89(5):907-914. 10.1038/sj.bjc.6601181, 2394481, 12942125.
43. Noh EJ, Kang SW, Shin YJ, Choi SH, Kim CG, Park IS, Wheatley DN, Min BH. Arginine deiminase enhances dexamethasone-induced cytotoxicity in human T-lymphoblastic leukemia CCRF-CEM cells. Int J Cancer 2004, 112(3):502-508. 10.1002/ijc.20435, 15382078.
44. Muerkoster S, Arlt A, Witt M, Gehrz A, Haye S, March C, Grohmann F, Wegehenkel K, Kalthoff H, Folsch UR, Schafer H. Usage of the NF-kappaB inhibitor sulfasalazine as sensitizing agent in combined chemotherapy of pancreatic cancer. Int J Cancer 2003, 104(4):469-476. 10.1002/ijc.10963, 12584745.
45. Greten FR, Weber CK, Greten TF, Schneider G, Wagner M, Adler G, Schmid RM. Stat3 and NF-kappaB activation prevents apoptosis in pancreatic carcinogenesis. Gastroenterology 2002, 123(6):2052-2063. 10.1053/gast.2002.37075, 12454861.
46. Kunnumakkara AB, Guha S, Krishnan S, Diagaradjane P, Gelovani J, Aggarwal BB. Curcumin potentiates antitumor activity of gemcitabine in an orthotopic model of pancreatic cancer through suppression of proliferation, angiogenesis, and inhibition of nuclear factor-kappaB-regulated gene products. Cancer Res 2007, 67(8):3853-3861. 10.1158/0008-5472.CAN-06-4257, 17440100.
47. Liptay S, Weber CK, Ludwig L, Wagner M, Adler G, Schmid RM. Mitogenic and antiapoptotic role of constitutive NF-kappaB/Rel activity in pancreatic cancer. Int J Cancer 2003, 105(6):735-746. 10.1002/ijc.11081, 12767057.
48. Xiong HQ, Abbruzzese JL, Lin E, Wang L, Zheng L, Xie K. NF-kappaB activity blockade impairs the angiogenic potential of human pancreatic cancer cells. Int J Cancer 2004, 108(2):181-188. 10.1002/ijc.11562, 14639600.
49. Yebra M, Filardo EJ, Bayna EM, Kawahara E, Becker JC, Cheresh DA. Induction of carcinoma cell migration on vitronectin by NF-kappa B-dependent gene expression. Mol Biol Cell 1995, 6(7):841-850. 10.1091/mbc.6.7.841, 301244, 7579698.
50. Loercher A, Lee TL, Ricker JL, Howard A, Geoghegen J, Chen Z, Sunwoo JB, Sitcheran R, Chuang EY, Mitchell JB, Baldwin AJ, Van Waes C. Nuclear factor-kappaB is an important modulator of the altered gene expression profile and malignant phenotype in squamous cell carcinoma. Cancer Res 2004, 64(18):6511-6523. 10.1158/0008-5472.CAN-04-0852, 15374962.
51. Ludwig L, Kessler H, Wagner M, Hoang-Vu C, Dralle H, Adler G, Bohm BO, Schmid RM. Nuclear factor-kappaB is constitutively active in C-cell carcinoma and required for RET-induced transformation. Cancer Res 2001, 61(11):4526-4535.
52. Maldonado V, Melendez-Zajgla J, Ortega A. Modulation of NF-kappa B, and Bcl-2 in apoptosis induced by cisplatin in HeLa cells. Mutat Res 1997, 381(1):67-75. 10.1016/S0027-5107(97)00150-4, 9403032.
53. Armstrong MB, Bian X, Liu Y, Subramanian C, Ratanaproeksa AB, Shao F, Yu VC, Kwok RP, Opipari AW, Castle VP. Signaling from p53 to NF-kappa B determines the chemotherapy responsiveness of neuroblastoma. Neoplasia 2006, 8(11):964-974. 1764827, 17215959.
54. Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC. Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis 2008, 29(1):147-156.